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Mapping the Aspergillus Niger Metabolite Biomarkers for in Situ and Early Evaluation of Table Grapes Contamination

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Mapping the Aspergillus Niger Metabolite Biomarkers for in Situ and Early Evaluation of Table Grapes Contamination Mapping the Aspergillus niger metabolite biomarkers for in situ and early evaluation of table grapes contamination João Raul Belinato State University of Campinas: Universidade Estadual de Campinas Carina Pedrosa Costa Universidade de Aveiro Adelaide Almeida Universidade de Aveiro Silvia Rocha Universidade de Aveiro Fabio Augusto ( [email protected] ) University of Campinas https://orcid.org/0000-0002-4673-0231 Research Article Keywords: Aspergillus niger, food contamination, GC×GC, metabolites, HS-SPME Posted Date: June 23rd, 2021 DOI: https://doi.org/10.21203/rs.3.rs-650006/v1 License: This work is licensed under a Creative Commons Attribution 4.0 International License. Read Full License Page 1/24 Abstract Aspergillus niger volatilome was recently explored using advanced gas chromatography tools tandem with multivariate analysis, which allowed to propose a molecular biomarker pattern for this fungus. A. niger is a ubiquitous fungus responsible for food contamination, being reported as one of the main agents of the black mold disease, a serious post-harvest pathology of table grapes. In this work the metabolite pattern already proposed was tested in three different conditions, i.e., by using : (i) 1 day of growth time for A. niger cultures; (ii) 1 day of growth time through A. niger cultures obtained from previously contaminated grapes and iii) in situ SPME approach directly on previously contaminated table grapes with A. niger. Supervised multivariate analysis was performed which revealed that after 1 day of inoculation it was possible to detect the A. niger biomarkers, which allows to infer its presence. Furthermore, the follow-up of this set of metabolites showed that they can be employed to conrm the presence of the pathogen in two varieties of table grapes. The results obtained conrm the potential applicability of the pattern of A. niger biomarkers to early detect the fungi (after 1 day of contamination) and also may be further explored for access food susceptibility to fungi contamination, based on a direct analysis of food item and taking advantage of the high sensitivity of the GC×GC-ToFMS. 1. Introduction Fungal contamination plays a major role in food spoilage and represents a problem which can result in huge economic losses, deterioration of food quality, reduction in nutrients availability, and contamination with compounds with high potential toxicity, such as mycotoxins(Finger et al. 2019). Mycotoxins are secondary metabolites produced by fungi that have adverse health effects on humans, animals, and crops. In this sense, prevention and control of these toxigenic fungi and mycotoxins in agricultural commodities have been priority objectives in food quality and safety (Bazioli et al. 2019; Gómez et al. 2019; Sun et al. 2020). Among different classes of food which are susceptible to fungal infection, the table grapes are very common case due to their thin pericarp and succulent esh. Thus, grapes can be easily contaminated with lamentous fungi in different steps across their production chain and for this reason, the quality control of table grapes must be very strict and effective (Li et al. 2017; Freire et al. 2018a). Some of the most relevant species related to the fungal infection of grapes are members of the genus Aspergillus (Freire et al. 2018a). Aspergillus niger is one of the main species responsible for contamination in grapes and derived products, promoting serious economic losses, being the distribution of black aspergilli in table grapes reported worldwide (Cano et al. 2015; Freire et al. 2020). The production of mycotoxins by A. niger is very known but the contribution to mycotoxin content in foodstuffs as well as the differences in production ability among species are controversial topics. Ochratoxin A is one of the metabolites usually associated to contamination by A. niger (Abarca et al. 2019; Dachery et al. 2019; Gómez et al. 2019; Santos-Ciscon et al. 2019), including in grapes (Freire et al. 2018b, 2020). However, as it is not specic for this species and therefore it cannot be used as a unambiguous biomarker. On the other hand, recent studies reported a set of metabolites that may be assigned as a A. niger biomarkers (Costa et al. 2016; Gil-Serna et al. 2019; Schueuermann et al. 2019). These reported metabolites are distributed in Page 2/24 different chemical families, such as aldehydes, ethers, alcohols, esters, ketones, hydrocarbons and terpenic compounds. Metabolic pathways such as amino acid metabolism, biosynthesis and metabolism of fatty acids, degradation of aromatic compounds, mono and sesquiterpenoid synthesis and carotenoid cleavage are found to be related to these set of compounds (Costa et al. 2016). Nevertheless, deeper studies of these metabolites production specically for A. niger are still not completely explored (Akhtar et al. 2015; Costa et al. 2016). Considering the importance of early diagnosis in food authentication and contamination, metabolomics enables the development of rapid and highly accurate molecular methods for the identication of the species. (Schloter et al. 1995; Järvinen et al. 2009; Xanthopoulou et al. 2018, 2019; Erban et al. 2019; Santos-Ciscon et al. 2019; Wang et al. 2019; Zhang et al. 2020; Fang et al. 2021). Microbial metabolomics represents a holistic approach for comprehensive monitoring of metabolites directly linked to cellular metabolism, providing an accurate snapshot of the microorganism metabolic prole and can be potentially useful for early detection (Fialho et al. 2010; Martins et al. 2017; de Souza et al. 2018a, b; Baptista et al. 2019). Untargeted microbial metabolomic approaches using mass spectrometry or mass spectroscopy- based analytical platforms have become extremely important in the last few years (Cubero-Leon et al. 2014; Schueuermann et al. 2019). Although it is very informative the whole metabolome studies can provide a huge volume of data. When it comes to detection of food contamination only a partial and signicant fraction of the metabolic prole is useful and desirable in order to detect the contaminant (Costa et al. 2016; Schueuermann et al. 2019). However, access to properly and interpretable data from microbe’s metabolite proles can be a real challenge due to the complexity of these samples. Therefore the use of high throughput and high sensitive analytical tools like comprehensive two dimensional gas chromatography (GC×GC) has been used in order to explore and extract useful data from microbial metabolome (Alves et al. 2015; Mousavi et al. 2016; Cardoso et al. 2017; Rees et al. 2017; de Souza et al. 2018b; Matos et al. 2019; Fonseca et al. 2020; Martins et al. 2020; Fang et al. 2021). GC×GC provides higher sensitivity and resolution when compared to conventional one-dimensional gas chromatography (1D-GC), which fulls the requirements for the analysis of complex biological samples. Also, GC×GC combined with time-of-ight mass spectrometry (ToFMS) increases sensitivity and detectability providing reliable identication of metabolites based on retention rates and mass spectra (de Souza et al. 2018c; Parastar et al. 2018; Carriço et al. 2020). 2. Materials And Methods 2.1. Fungal strains and culture growth conditions The three fungal strains used in this study - Aspergillus niger (GenBank accession number KT964850), Penicillium chrysogenum (GenBank accession number KT799549) and Candida albicans (GenBank accession number SC5314) - were obtained from the Department of Biology, University of Aveiro, Portugal. Fresh cultures were prepared by inoculation on Yeast Glucose Chloramphenicol Agar (YGCA − 20 g L − 1 D- glucose, 5 g L− 1 yeast extract, 0.1 g L− 1 chloramphenicol and 18 g L− 1 agar; Liolchem®, Italy). Page 3/24 The rst experiment was conducted following the same protocol already published for the three fungal strains (Costa et al. 2016) and adapted in the current study for one day of growth after the inoculation as the workow presented in Fig. 1–(a). Five plates were prepared with solid YGCA for each assay, where the three fungi were inoculated separately. All essays were performed in triplicate. Each experiment was repeated for 7 days in order to provide replicates at different times (i.e., three strains with 1-day growth, repeated for 7 days). For each assay, the sampling was performed by adding 10 mL of Ringer solution (Merck Millipore) per plate (5 plates per assay) to collect the cellular content of each sample. After that, 50 mL of the suspension were collected from each assay, an aliquot of 25 mL was collected to volatile metabolites proling and other aliquot of 25 mL for the determination of cell concentration. The cell concentration was expressed as colony-forming units per milliliter (CFU mL− 1). The homogenized suspension was serially diluted in Ringer solution and aliquots of 100 µL were spread on YGCA (5 replicates per dilution). These results were employed to normalize the total areas of each chemical feature detected, therefore allowing the determination of specic metabolite production per cell. Finally, to assess general distinction based on metabolomics data, P. chrysogenum and C. albicans were also plated onto YGCA at 25°C also performing 5 plates for each assay under study (in a total of 15 plates per condition corresponding to 3 independents assays) and the same procedure which for A. niger samples in solid media mentioned above was applied. Penicillium chrysogenum was chosen to compare two lamentous fungi, though from different species, and Candida albicans was selected for its importance among immunocompromised patients within clinical setting. 2.2. Grapes contamination protocol Red globe and Dominga table grapes (Vitis vinifera) in the commercial mature stage were obtained at the local market in Aveiro, Portugal. The grapes were washed, supercially disinfected with 0.2% (v/v) sodium hypochlorite for 3 min and rinsed in distilled water to eliminate the residual sodium hypochlorite after being removed from the stems. After drying, the fruits were wounded in a 2 mm depth and 10 µL of an A. niger conidial suspension (1×105 conidia/mL) was inoculated in the wounded area.
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